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Effects of Metal Toxicity on the Early Life Stages of The EFFECTS OF METAL TOXICITY ON THE EARLY LIFE STAGES OF THE SEA URCHIN EVECHINUS CHLOROTICUS By Agnes Mireille Rouchon A thesis submitted to the Victoria University of Wellington in fulfilment of the requirements for the degree of Doctor of Philosophy in Marine Biology 2015 To my Dad, for countless hours spent looking at snails, snakes, and other critters; this is how it all began… À mon Papa, pour toutes ces heures passées à observer escargots, serpents et autres bestioles; c’est comme ça que tout a commencé… i ii ABSTRACT Metals are a common source of pollution in coastal waters, and have long been recognised as a major concern for many marine species, especially their early life stages. Although effects have been examined using standard toxicity assays, the impact of metals in more complex and realistic exposure regimes is still poorly known, in particular with regards to latent effects across multiple life stages and the interaction of multiple stressors. In this thesis, the effects of metals were investigated for multiple life stages of the endemic New Zealand sea urchin Evechinus chloroticus. Standard short-term bioassays were performed on the early life stage of E. chloroticus and also the endemic abalone Haliotis iris, for comparison. These assays evaluated the toxicity of three major pollutants (copper, lead and zinc) alone and in combination, on these species. Embryos of both species were highly vulnerable to copper (EC50s: 5.4 and 3.4 µg/L respectively for E. chloroticus and H. iris) and zinc (27.7 and 13.1 µg/L) but relatively tolerant to lead (52.2 and 775 µg/L), and there was no evidence of synergistic effects of metal mixtures. The latent effects of copper across two life stages in E. chloroticus, larval and juvenile, were investigated with laboratory experiments using realistic scenarios of low copper concentration, short pulses of exposure and examining exposure through dietary intake as well as waterborne exposure. Strong latent and carry-over effects were observed even at low concentration and short exposure time. For example, individuals exposed as larvae to 10.4 µg/L Cu for two days developed normally during the larval stage but had strongly impaired subsequent growth, with average body size decreasing by 24% in the 25 d following settlement. Moreover, juveniles previously exposed to copper as larvae were less resistant to a subsequent exposure, with up to four times higher mortality. Latent effects were especially important when copper was present in the diet rather than dissolved in water. For example, E. chloroticus larvae exposed to 2.3 µg/L Cu in water and fed with an algal diet cultured in the same concentration had a settlement success three times lower than those exposed only to waterborne copper. Furthermore, a short pulse exposure (4 days) to copper in the algal diet was generally more toxic than chronic exposure, showing that iii a short-lived bloom of contaminated phytoplankton may have a more severe impact on zooplankton than chronic pollution. Because metal discharge in coastal water is generally associated with freshwater (e.g. storm water or river plumes), the toxicity of copper was evaluated in both normal and low salinity seawater. Low salinity (24 ppt) increased copper toxicity in E. chloroticus larvae under chronic exposure to high levels (15 µg/L; 43% and 80% lower survival and normal development rate, respectively) but not under a single pulse exposure (4 days) to low concentration (5 µg/L). This highlights the importance of using realistic exposure in laboratory assays. Finally, the effect of copper on adult E. chloroticus and in particular on their fertilisation success was evaluated. Strong sublethal effects were observed after exposure to 50 µg/L Cu for two weeks including spawning impairment (especially in females) and elevated copper burden in gonads (25-times higher than control animals). However, the fertilisation success of successfully spawning males was not affected. The prevalence of local metal contamination was also measured at the mouth of local river plumes and in E. chloroticus gonads at sites expected to vary in likely exposure to pollution. Copper levels exceeding water quality criteria were found in two instances in coastal agricultural runoff (Makara stream). Other metals were within water quality cirteria in all samplings. Adult E. chloroticus had an elevated copper burden in gonads in an urban site compared to a control site (0.77 µg/g vs. 0.27 µg/g). In total, this research demonstrates the need for considering toxic effects across multiple life stages and using realistic exposure regimes (e.g. timing, concentration, multiple stressors) to better understand the likely impact of metal pollution on marine populations. It also provides the first measure of metal toxicity on early life stages of an endemic species of cultural and commercial importance in New Zealand. iv ACKNOWLEDGEMENTS First and foremost, my deepest gratitude to Nicolas Gilbert for being my anchor in the sometimes stormy sea of graduate research, for his amazing problem-solving skills that truly contributed to the quality of this thesis, and, of course, for IT support. I am very grateful to my supervisor Nicole Phillips, for providing great feedback, encouragements when I needed them, and for being always supportive (even when life got in the way). Thanks to my secondary supervisor Simon Davy for advice and comments. Many thanks to Sonja Miller for invaluable help in getting me started and advice and encouragements along the way. Special thanks to Fernanda Piraud, Ursula Rojas Nazar and Alix LaFerriere for friendship and much needed support while writing and facing the challenges of combining motherhood and PhD study. Thanks to Camille Poutrin, Katie Clemens and Jenifer Howe for great help in the lab when it was most needed. Thanks to John van der Sman for help in building experimental apparatus. Thanks to my many helpers in the field: Paul Mensink, Jenny Oliver, Shane Geange, Cesar Cardenas Alacorn, Abi Powell, Sonja Miller, John van der Sman, Daniel McNaughtan, Simona Boschetti, Ursula Rojas Nazar, Christian Carrizo, Mauricio Cifuentes, Peter Edward; and in the lab: Fernanda Piraud, Richard Crerar, Steven Walton, Charlotte Dohrn, Laura, Nicolas Gilbert and Jean-Paul Rouchon. v Thanks to Sonja Miller, Peter Edward and Taputu Raea for their help in keeping my broodstock well fed and happy. Many thanks to all the VUCELers who made this journey so much fun. Thanks for all the stimulating conversations, friendships and morning teas! I would like to acknowledge the Victoria Doctoral Scholarship, Victoria PhD Submission Scholarship and the Greater Wellington Regional Council for funding. I am grateful to Graeme Moss and NIWA’s Mahanga Bay Lab for generous use of their facilities and paua broodstock. Thanks to Sharon van Soest from Environmental Laboratories Services in Petone for training on spectrometry techniques. Many thanks to Gordon Heeley and Victoria University School of Chemical and Physical Sciences for letting me use their brand new GFAA. And a huge thank you to my family in Reunion Island, France and Quebec for their love and support. Special thanks to my parents and parents-in-law for their help with babysitting, to my Mum for always been here to listen to my endless talks about my critters (“they are so cuuute!”), experiments, or other science-related subjects over the years, and, finally, to my beloved daughter who made the journey both so much more challenging and so much more worthwhile. vi CONTENTS Abstract ............................................................................................................................ iii Acknowledgements .......................................................................................................... v Contents .......................................................................................................................... vii List of Tables ................................................................................................................. xiii List of Figures ............................................................................................................... xvii List of Abbreviations and Acronyms ............................................................................. xxi CHAPTER 1 General Introduction .............................................................................. 1 1.1 Coastal benthic organisms ...................................................................................... 1 1.2 Prevalence of metal pollution worldwide ............................................................... 2 1.3 Mechanisms of toxicity ........................................................................................... 4 1.3.1 Bioavailability ................................................................................................. 4 1.3.2 Copper ............................................................................................................. 4 1.3.3 Zinc .................................................................................................................. 5 1.3.4 Lead ................................................................................................................. 5 1.4 Impacts of metal pollution on marine species ........................................................ 5 1.5 How to evaluate the impact of these stressors? ...................................................... 7 1.5.1 Interaction between stressors .........................................................................
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